Rats Answer an Unexpected Question after Incidental Encoding
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A fundamental aspect of episodic memory is that retrieval of information can occur when encoding is incidental and memory assessment is unexpected. These features are difficult to model in animals because behavioral training likely gives rise to well-learned expectations about the sequence of events. Thus, the possibility remains that animals may solve an episodic memory test by using well-learned semantic rules without remembering the episode at memory assessment. Here we show that rats can answer an unexpected question after incidental encoding in a hippocampal-dependent manner, consistent with the use of episodic memory. Rats were initially trained to report about a recent event (food versus no food) and separately searched for food where there was no expectation of being asked about the presence of food. To test episodic memory, we gave rats the opportunity to incidentally encode the presence or absence of food and unexpectedly asked them to report about the recent event. Temporary inactivation of the CA3 region of the hippocampus with bilateral infusions of lidocaine selectively eliminated the ability of rats to answer the unexpected, but not the expected, question. Our studies suggest that rats remember an earlier episode after incidental encoding based upon hippocampal-dependent episodic memory.
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When information is encoded incidentally and subsequently tested in an unexpected memory assessment, the transformation of this information into a preselected future action is impossible.
“By contrast, when information is encoded incidentally and subsequently tested in an unexpected memory assessment, the transformation of this information into a preselected future action is impossible [79,82,85,90]”
From Is episodic-like memory <i>like</i> episodic memory? (2024) · cites this paper as [82]
Training animals to explicitly encode and report information in an anticipated memory test may result in the application of non-episodic mechanisms to solve these tasks.
“That said, training animals to explicitly encode and report information in an anticipated memory test, as is required for what–where–when memory experiments, may result in the application of non-episodic mechanisms to solve these tasks [74,79–84].”
From Is episodic-like memory <i>like</i> episodic memory? (2024) · cites this paper as [82]
Rodents with hippocampal lesions fail in both what-where-when tasks and incidental encoding tasks.
“These observations are supported by research using established episodic-like memory paradigms, showing that rodents with hippocampal lesions fail in both what–where–when tasks [70,72] as well as incidental encoding tasks [82].”
From Is episodic-like memory <i>like</i> episodic memory? (2024) · cites this paper as [82]
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Crystal, J. D. (2024) · Current Biology · doi:10.1016/j.cub.2024.07.027 · Cited by 1 · see citing works
Self-citationNaeem, S., Najam, R., Alam, N., & Akhter, S. W. (2016) · Advances in Parkinson s Disease · doi:10.4236/apd.2016.52003 · Cited by 1 · see citing works
Motivational Neuroscience: Instant Desire for Something You Know Is Bad
Crystal, J. D. (2013) · Current Biology · doi:10.1016/j.cub.2013.01.060
Self-citationMyroshnychenko, M., & Lapish, C. C. (2015) · BMC Neuroscience · doi:10.1186/1471-2202-16-s1-p139
Report Source Memory in the Rat
Crystal, J. D., Alford, W. T., Zhou, W., & Hohmann, A. G. (2013)
Self-citationEpisodic-like Memory in Dogs: Solving What-Where-When Tasks
Lo, K. H. (2018) · Scholarship@Western (Western University)
Neuroscience: Memory Encoding in the Absence of Cell Firing
Crystal, J. D. (2018) · Current Biology · doi:10.1016/j.cub.2018.08.007
Self-citationKaufman, A. B., Call, J., & Kaufman, J. C. (2021) · Cambridge University Press eBooks · doi:10.1017/9781108564113.008
Crystal, J. D. (2017) · Springer eBooks · doi:10.1007/978-3-319-47829-6_956-1
Self-citation(2022) · Cambridge University Press eBooks · doi:10.1017/9781108768450.019
Crystal, J. D. (2022) · Springer eBooks · doi:10.1007/978-3-319-55065-7_956
Self-citationBillard, P., Clayton, N. S., & Jozet‐Alves, C. (2022) · Springer eBooks · doi:10.1007/978-3-319-55065-7_1770
Incidental Temporal Binding in Rats: A Novel Behavioral Task Relevant to Episodic MemoryPreprint
Radostová, D., Kunčická, D., Krajčovič, B., Hejtmánek, L., Petrásek, T., Svoboda, J., Stuchlı́k, A., & Brožka, H. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.08.30.505895
Memory for where and when: pigeons use single-code/default strategy
Zentall, T. R., & Peng, D. N. (2023) · Learning & Behavior · doi:10.3758/s13420-023-00607-y
Zentall, T. R. (2025) · Translational Neuroscience · doi:10.1515/tnsci-2025-0383
Crystal, J. D. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-29068-8.00188-4
Self-citation
- Authors
- Zhou, W., Hohmann, A. G., & Crystal, J. D.
- Affiliations
- Indiana University Bloomington (US)
- Corresponding author
- Crystal, Jonathon D.
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2012-06
- Volume
- 22
- Issue
- 12
- Pages
- 1149-1153
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC3376895
- OpenAlex
- W2074887182
- Cited by
- 98
- References
- 29
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 11 · 2023: 4 · 2022: 10 · 2021: 8 · 2020: 5 · 2019: 10 · 2018: 8 · 2017: 5 · 2016: 7 · 2015: 7 · 2014: 4 · 2013: 9 · 2012: 3
- FWCI
- 3.76
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Indiana University Bloomington
- National Institute of Mental Health (R01MH080052)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Keywords
- episodic memory, incidental encoding, hippocampus, CA3, lidocaine inactivation, rats, semantic rules, memory assessment
- MeSH terms
- Animals, Association Learning, Choice Behavior, Hippocampus, Lidocaine, Male, Mental Recall, Maze Learning, Rats, Long-Evans, Rats, Memory, Episodic
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